Author Correction: Global status and conservation potential of reef sharks.

An Amendment to this paper has been published and can be accessed via a link at the top of the paper.

Global status and conservation potential of reef sharks.

Decades of overexploitation have devastated shark populations, leaving considerable doubt as to their ecological status1,2. Yet much of what is known about sharks has been inferred from catch records in industrial fisheries, whereas far less information is available about sharks that live in coastal habitats3. Here we address this knowledge gap using data from more than 15,000 standardized baited remote underwater video stations that were deployed on 371 reefs in 58 nations to estimate the conservation status of reef sharks globally. Our results reveal the profound impact that fishing has had on reef shark populations: we observed no sharks on almost 20% of the surveyed reefs. Reef sharks were almost completely absent from reefs in several nations, and shark depletion was strongly related to socio-economic conditions such as the size and proximity of the nearest market, poor governance and the density of the human population. However, opportunities for the conservation of reef sharks remain: shark sanctuaries, closed areas, catch limits and an absence of gillnets and longlines were associated with a substantially higher relative abundance of reef sharks. These results reveal several policy pathways for the restoration and management of reef shark populations, from direct top-down management of fishing to indirect improvement of governance conditions. Reef shark populations will only have a high chance of recovery by engaging key socio-economic aspects of tropical fisheries.

A large-scale experiment finds no evidence that a seismic survey impacts a demersal fish fauna.

Seismic surveys are used to locate oil and gas reserves below the seabed and can be a major source of noise in marine environments. Their effects on commercial fisheries are a subject of debate, with experimental studies often producing results that are difficult to interpret. We overcame these issues in a large-scale experiment that quantified the impacts of exposure to a commercial seismic source on an assemblage of tropical demersal fishes targeted by commercial fisheries on the North West Shelf of Western Australia. We show that there were no short-term (days) or long-term (months) effects of exposure on the composition, abundance, size structure, behavior, or movement of this fauna. These multiple lines of evidence suggest that seismic surveys have little impact on demersal fishes in this environment.

Scaling of Activity Space in Marine Organisms across Latitudinal Gradients.

AbstractUnifying models have shown that the amount of space used by animals (e.g., activity space, home range) scales allometrically with body mass for terrestrial taxa; however, such relationships are far less clear for marine species. We compiled movement data from 1,596 individuals across 79 taxa collected using a continental passive acoustic telemetry network of acoustic receivers to assess allometric scaling of activity space. We found that ectothermic marine taxa do exhibit allometric scaling for activity space, with an overall scaling exponent of 0.64. However, body mass alone explained only 35% of the variation, with the remaining variation best explained by trophic position for teleosts and latitude for sharks, rays, and marine reptiles. Taxon-specific allometric relationships highlighted weaker scaling exponents among teleost fish species (0.07) than sharks (0.96), rays (0.55), and marine reptiles (0.57). The allometric scaling relationship and scaling exponents for the marine taxonomic groups examined were lower than those reported from studies that had collated both marine and terrestrial species data derived using various tracking methods. We propose that these disparities arise because previous work integrated summarized data across many studies that used differing methods for collecting and quantifying activity space, introducing considerable uncertainty into slope estimates. Our findings highlight the benefit of using large-scale, coordinated animal biotelemetry networks to address cross-taxa evolutionary and ecological questions.

Effects of human footprint and biophysical factors on the body-size structure of fished marine species.

Marine fisheries in coastal ecosystems in many areas of the world have historically removed large-bodied individuals, potentially impairing ecosystem functioning and the long-term sustainability of fish populations. Reporting on size-based indicators that link to food-web structure can contribute to ecosystem-based management, but the application of these indicators over large (cross-ecosystem) geographical scales has been limited to either fisheries-dependent catch data or diver-based methods restricted to shallow waters (<20 m) that can misrepresent the abundance of large-bodied fished species. We obtained data on the body-size structure of 82 recreationally or commercially targeted marine demersal teleosts from 2904 deployments of baited remote underwater stereo-video (stereo-BRUV). Sampling was at up to 50 m depth and covered approximately 10,000 km of the continental shelf of Australia. Seascape relief, water depth, and human gravity (i.e., a proxy of human impacts) were the strongest predictors of the probability of occurrence of large fishes and the abundance of fishes above the minimum legal size of capture. No-take marine reserves had a positive effect on the abundance of fishes above legal size, although the effect varied across species groups. In contrast, sublegal fishes were best predicted by gradients in sea surface temperature (mean and variance). In areas of low human impact, large fishes were about three times more likely to be encountered and fishes of legal size were approximately five times more abundant. For conspicuous species groups with contrasting habitat, environmental, and biogeographic affinities, abundance of legal-size fishes typically declined as human impact increased. Our large-scale quantitative analyses highlight the combined importance of seascape complexity, regions with low human footprint, and no-take marine reserves in protecting large-bodied fishes across a broad range of species and ecosystem configurations.

Las pesquerías marinas de los ecosistemas costeros en muchas áreas del mundo históricamente han removido a individuos de gran tamaño, potencialmente perjudicando el funcionamiento ambiental y la sostenibilidad a largo plazo de las poblaciones de peces. Los reportes sobre los indicadores basados en el tamaño que se vinculan con la estructura de la red alimenticia pueden contribuir al manejo basado en el ecosistema, aunque la aplicación de estos indicadores a grandes (inter-ecosistemas) escalas geográficas ha estado limitada a datos de captura dependientes de las pesquerías o métodos basados en el buceo restringidos a aguas someras (<20 m), lo cual puede representar erróneamente la abundancia de peces de gran tamaño capturados para la pesca. Obtuvimos los datos de la estructura del tamaño corporal de 82 teleósteos marinos demersales focalizados por razones recreativas o comerciales tomados de 2,904 despliegues de video estéreo subacuático remoto con cebo (stereo-BRUV, en inglés). El muestreo se realizó hasta los 50 metros de profundidad y abarcó aproximadamente 10,000 km del talud continental de Australia. El relieve marino, la profundidad del agua y la gravedad humana (es decir, un indicador de los impactos humanos) fueron los pronosticadores más sólidos de la probabilidad de incidencia de los peces de gran tamaño y de la abundancia de peces por encima del tamaño legal mínimo de captura. Las reservas marinas de protección total tienen un efecto positivo sobre la abundancia de los peces que están por encima del tamaño legal, aunque el efecto varió según el grupo de especies. Como contraste, los peces de tamaño sublegal fueron pronosticados de mejor manera usando gradientes de la temperatura de la superficie marina (media y varianza). En las áreas con un impacto humano reducido, los peces de gran tamaño corporal tenían hasta tres veces mayor probabilidad de aparecer y los peces de tamaño legal eran aproximadamente cinco veces más abundantes. Para los grupos de especies conspicuas con afinidades contrastantes de hábitat, ambiente y biogeografía, la abundancia de peces de tamaño legal normalmente declinó conforme aumentó el impacto humano. Nuestros análisis cuantitativos a gran escala resaltan la importancia conjunta que tienen la complejidad marina, las regiones con una huella humana reducida y las reservas marinas de protección total para la protección de los peces de gran tamaño corporal en una extensa gama de especies y configuraciones ecosistémicas. Efectos de la Huella Humana y los Factores Biofísicos sobre la Estructura del Tamaño Corporal de Especies Marinas Capturadas para la Pesca.

Increased connectivity and depth improve the effectiveness of marine reserves.

Marine reserves are a key tool for the conservation of marine biodiversity, yet only ~2.5% of the world's oceans are protected. The integration of marine reserves into connected networks representing all habitats has been encouraged by international agreements, yet the benefits of this design has not been tested empirically. Australia has one of the largest systems of marine reserves, providing a rare opportunity to assess how connectivity influences conservation success. An Australia-wide dataset was collected using baited remote underwater video systems deployed across a depth range from 0 to 100 m to assess the effectiveness of marine reserves for protecting teleosts subject to commercial and recreational fishing. A meta-analytical comparison of 73 fished species within 91 marine reserves found that, on average, marine reserves had 28% greater abundance and 53% greater biomass of fished species compared to adjacent areas open to fishing. However, benefits of protection were not observed across all reserves (heterogeneity), so full subsets generalized additive modelling was used to consider factors that influence marine reserve effectiveness, including distance-based and ecological metrics of connectivity among reserves. Our results suggest that increased connectivity and depth improve the aforementioned marine reserve benefits and that these factors should be considered to optimize such benefits over time. We provide important guidance on factors to consider when implementing marine reserves for the purpose of increasing the abundance and size of fished species, given the expected increase in coverage globally. We show that marine reserves that are highly protected (no-take) and designed to optimize connectivity, size and depth range can provide an effective conservation strategy for fished species in temperate and tropical waters within an overarching marine biodiversity conservation framework.

Offshore oil and gas infrastructure plays a minor role in marine metapopulation dynamics.

Decommissioning consequences of offshore oil and gas infrastructure removal on marine population dynamics, including connectivity, are not well understood. We modelled the connectivity and metapopulation dynamics of three fish and two benthic invertebrate species inhabiting the natural rocky reefs and offshore oil and gas infrastructure located in the Bass Strait, south-east Australia. Using a network approach, we found that platforms are not major sources, destinations, or stepping-stones for most species, yet act as modest sources for connectivity of Corynactis australis (jewel anemone). In contrast, sections of subsea pipelines appear to act as stepping-stones, source and destination habitats of varying strengths for all study species, except for Centrostephanus rodgersii (long-spined sea urchin). Natural reefs were the main stepping-stones, local source, and destination habitats for all study species. These reefs were largely responsible for the overall metapopulation growth of all study species (average of 96 % contribution across all species), with infrastructure acting as a minor contributor (<2 % average contribution). Full or partial decommissioning of platforms should have a very low or negligible impact on the overall metapopulation dynamics of the species explored, except C. australis, while full removal of pipelines could have a low impact on the metapopulation dynamics of benthic invertebrate species and a moderate impact on fish species (up to 34.1 % reduction in the metapopulation growth). We recommend that the decision to remove offshore infrastructure, either in full or in-part, be made on a platform-by-platform basis and consider contributions of pipelines to connectivity and metapopulation dynamics.

A large-scale experiment finds no consistent evidence of change in mortality or commercial productivity in silverlip pearl oysters (Pinctada maxima) exposed to a seismic source survey.

High-intensity, impulsive sounds are used to locate oil and gas reserves during seismic exploration of the seafloor. The impacts of this noise pollution on the health and mortality of marine invertebrates are not well known, including the silverlip pearl oyster (Pinctada maxima), which comprises one of the world's last remaining significant wildstock pearl oyster fisheries, in northwestern Australia. We exposed ≈11,000 P. maxima to a four-day experimental seismic survey, plus one vessel-control day. After exposure, survival rates were monitored throughout a full two-year production cycle, and the number and quality of pearls produced at harvest were assessed. Oysters from two groups, on one sampling day, exhibited reduced survival and pearl productivity compared to controls, but 14 other groups receiving similar or higher exposure levels did not. We therefore found no conclusive evidence of an impact of the seismic source survey on oyster mortality or pearl production.

Directed conservation of the world's reef sharks and rays.

Many shark populations are in decline around the world, with severe ecological and economic consequences. Fisheries management and marine protected areas (MPAs) have both been heralded as solutions. However, the effectiveness of MPAs alone is questionable, particularly for globally threatened sharks and rays ('elasmobranchs'), with little known about how fisheries management and MPAs interact to conserve these species. Here we use a dedicated global survey of coral reef elasmobranchs to assess 66 fully protected areas embedded within a range of fisheries management regimes across 36 countries. We show that conservation benefits were primarily for reef-associated sharks, which were twice as abundant in fully protected areas compared with areas open to fishing. Conservation benefits were greatest in large protected areas that incorporate distinct reefs. However, the same benefits were not evident for rays or wide-ranging sharks that are both economically and ecologically important while also threatened with extinction. We show that conservation benefits from fully protected areas are close to doubled when embedded within areas of effective fisheries management, highlighting the importance of a mixed management approach of both effective fisheries management and well-designed fully protected areas to conserve tropical elasmobranch assemblages globally.

Widespread diversity deficits of coral reef sharks and rays.

A global survey of coral reefs reveals that overfishing is driving resident shark species toward extinction, causing diversity deficits in reef elasmobranch (shark and ray) assemblages. Our species-level analysis revealed global declines of 60 to 73% for five common resident reef shark species and that individual shark species were not detected at 34 to 47% of surveyed reefs. As reefs become more shark-depleted, rays begin to dominate assemblages. Shark-dominated assemblages persist in wealthy nations with strong governance and in highly protected areas, whereas poverty, weak governance, and a lack of shark management are associated with depauperate assemblages mainly composed of rays. Without action to address these diversity deficits, loss of ecological function and ecosystem services will increasingly affect human communities.

Isolated reefs support stable fish communities with high abundances of regionally fished species.

Anthropogenic impacts at isolated and inaccessible reefs are often minimal, offering rare opportunities to observe fish assemblages in a relatively undisturbed state. The remote Rowley Shoals are regarded as one of the healthiest reef systems in the Indian Ocean with demonstrated resilience to natural disturbance, no permanent human population nearby, low visitation rates, and large protected areas where fishing prohibitions are enforced. We used baited remote underwater video systems (BRUVS) to quantify fish assemblages and the relative abundance of regionally fished species within the lagoon, on the slope and in the mesophotic habitat at the Rowley Shoals at three times spanning 14 years and compared abundances of regionally fished species and the length distributions of predatory species to other isolated reefs in the northeast Indian Ocean. Fish assemblage composition and the relative abundance of regionally fished species were remarkably stable through time. We recorded high abundances of regionally fished species relative to other isolated reefs, including globally threatened humphead Maori wrasse (Cheilinus undulatus) and bumphead parrotfish (Bolbometopon muricatum). Length distributions of fish differed among habitats at the Rowley Shoals, suggesting differences in ontogenetic shifts among species. The Cocos (Keeling) Islands typically had larger-bodied predatory species than at the Rowley Shoals. Differences in geomorphology, lagoonal habitats, and fishing history likely contribute to the differences among remote reefs. Rowley Shoals is a rare example of a reef system demonstrating ecological stability in reef fish assemblages during a time of unprecedented degradation of coral reefs.

Moray eels are more common on coral reefs subject to higher human pressure in the greater Caribbean.

Proximity and size of the nearest market ('market gravity') have been shown to have strong negative effects on coral reef fish communities that can be mitigated by the establishment of closed areas. However, moray eels are functionally unique predators that are generally not subject to targeted fishing and should therefore not directly be affected by these factors. We used baited remote underwater video systems to investigate associations between morays and anthropogenic, habitat, and ecological factors in the Caribbean region. Market gravity had a positive effect on morays, while the opposite pattern was observed in a predator group subject to exploitation (sharks). Environmental DNA analyses corroborated the positive effect of market gravity on morays. We hypothesize that the observed pattern could be the indirect result of the depletion of moray competitors and predators near humans.

Protection from illegal fishing and shark recovery restructures mesopredatory fish communities on a coral reef.

The recovery of communities of predatory fishes within a no-take marine reserve after the eradication of illegal fishing provides an opportunity to examine the role of sharks and other large-bodied mesopredatory fishes in structuring reef fish communities. We used baited remote underwater video stations to investigate whether an increase in sharks was associated with a change in structure of the mesopredatory fish community at Ashmore Reef, Western Australia. We found an almost fourfold increase in shark abundance in reef habitat from 0.64 hr-1 ± 0.15 SE in 2004, when Ashmore Reef was being fished illegally, to 2.45 hr-1 ± 0.37 in 2016, after eight years of full-time enforcement of the reserve. Shark recovery in reef habitat was accompanied by a two and a half-fold decline in the abundance of small mesopredatory fishes (≤50 cm TL) (14.00 hr-1 ± 3.79 to 5.6 hr-1 ± 1.20) and a concomitant increase in large mesopredatory fishes (≥100 cm TL) from 1.82 hr-1 ± 0.48 to 4.27 hr-1 ± 0.93. In contrast, near-reef habitats showed an increase in abundance of large mesopredatory fishes between years (2.00 hr-1 ± 0.65 to 4.56 hr-1 ± 1.11), although only smaller increases in sharks (0.67 hr-1 ± 0.25 to 1.22 hr-1 ± 0.34) and smaller mesopredatory fishes. Although the abundance of most mesopredatory groups increased with recovery from fishing, we suggest that the large decline of small mesopredatory fish in reef habitat was mostly due to higher predation pressure following the increase in sharks and large mesopredatory fishes. At the regional scale, the structure of fished communities at Ashmore Reef in 2004 resembled those of present day Scott Reefs, where fishing still continues today. In 2016, Ashmore fish communities resembled those of the Rowley Shoals, which have been protected from fishing for decades.

Spot the match - wildlife photo-identification using information theory.

BACKGROUND: Effective approaches for the management and conservation of wildlife populations require a sound knowledge of population demographics, and this is often only possible through mark-recapture studies. We applied an automated spot-recognition program (I3S) for matching natural markings of wildlife that is based on a novel information-theoretic approach to incorporate matching uncertainty. Using a photo-identification database of whale sharks (Rhincodon typus) as an example case, the information criterion (IC) algorithm we developed resulted in a parsimonious ranking of potential matches of individuals in an image library. Automated matches were compared to manual-matching results to test the performance of the software and algorithm. RESULTS: Validation of matched and non-matched images provided a threshold IC weight (approximately 0.2) below which match certainty was not assured. Most images tested were assigned correctly; however, scores for the by-eye comparison were lower than expected, possibly due to the low sample size. The effect of increasing horizontal angle of sharks in images reduced matching likelihood considerably. There was a negative linear relationship between the number of matching spot pairs and matching score, but this relationship disappeared when using the IC algorithm. CONCLUSION: The software and use of easily applied information-theoretic scores of match parsimony provide a reliable and freely available method for individual identification of wildlife, with wide applications and the potential to improve mark-recapture studies without resorting to invasive marking techniques.

Coral reproduction in Western Australia.

Larval production and recruitment underpin the maintenance of coral populations, but these early life history stages are vulnerable to extreme variation in physical conditions. Environmental managers aim to minimise human impacts during significant periods of larval production and recruitment on reefs, but doing so requires knowledge of the modes and timing of coral reproduction. Most corals are hermaphroditic or gonochoric, with a brooding or broadcast spawning mode of reproduction. Brooding corals are a significant component of some reefs and produce larvae over consecutive months. Broadcast spawning corals are more common and display considerable variation in their patterns of spawning among reefs. Highly synchronous spawning can occur on reefs around Australia, particularly on the Great Barrier Reef. On Australia's remote north-west coast there have been fewer studies of coral reproduction. The recent industrial expansion into these regions has facilitated research, but the associated data are often contained within confidential reports. Here we combine information in this grey-literature with that available publicly to update our knowledge of coral reproduction in WA, for tens of thousands of corals and hundreds of species from over a dozen reefs spanning 20° of latitude. We identified broad patterns in coral reproduction, but more detailed insights were hindered by biased sampling; most studies focused on species of Acropora sampled over a few months at several reefs. Within the existing data, there was a latitudinal gradient in spawning activity among seasons, with mass spawning during autumn occurring on all reefs (but the temperate south-west). Participation in a smaller, multi-specific spawning during spring decreased from approximately one quarter of corals on the Kimberley Oceanic reefs to little participation at Ningaloo. Within these seasons, spawning was concentrated in March and/or April, and October and/or November, depending on the timing of the full moon. The timing of the full moon determined whether spawning was split over two months, which was common on tropical reefs. There were few data available for non-Acropora corals, which may have different patterns of reproduction. For example, the massive Porites seemed to spawn through spring to autumn on Kimberley Oceanic reefs and during summer in the Pilbara region, where other common corals (e.g. Turbinaria & Pavona) also displayed different patterns of reproduction to the Acropora. The brooding corals (Isopora & Seriatopora) on Kimberley Oceanic reefs appeared to planulate during many months, possibly with peaks from spring to autumn; a similar pattern is likely on other WA reefs. Gaps in knowledge were also due to the difficulty in identifying species and issues with methodology. We briefly discuss some of these issues and suggest an approach to quantifying variation in reproductive output throughout a year.

Growth of tropical Dasyatid rays estimated using a multi-analytical approach.

We studied the age and growth of four sympatric stingrays: reticulate whipray, Himanutra uarnak (n=19); blue mask, Neotrygon kuhlii (n=34); cowtail, Pastinachus atrus (n=32) and blue-spotted fantail, Taeniura lymma (n=40) rays at Ningaloo Reef, a fringing coral reef on the north-western coast of western Australia. Age estimates derived from band counts within sectioned vertebrae ranged between 1 and 27 years (H. uarnak, 1 - 25 yrs.; N. kuhlii, 1.5 - 13 yrs.; P. atrus, 1 - 27 yrs. and T. lymma, 1 -11 yrs.). Due to limitations of sample sizes, we combined several analytical methods for estimating growth parameters. First, we used nonlinear least squares (NLS) to identify the growth model that best fitted the data. We then used this model, prior information and the data within a Bayesian framework to approximate the posterior distribution of the growth parameters. For all species the two-parameter von Bertalanffy growth model provided the best fit to size-at-age datasets. Based on this model, the Bayesian approach allowed the estimation of median values of W(D∞) (cm) and k (yr(-1)) for the four species (H. uarnak: 149 and 0.12; N. kuhlii: 42 and 0.38; P. atrus 156 and 0.16, and T. lymma 33 and 0.24, respectively). Our approach highlights the value of combining different analytical methods and prior knowledge for estimating growth parameters when data quality and quantity are limited.

Environmental influences on patterns of vertical movement and site fidelity of grey reef sharks (Carcharhinus amblyrhynchos) at aggregation sites.

We used acoustic telemetry to describe the patterns of vertical movement, site fidelity and residency of grey reef sharks (Carcharhinus amblyrhynchos) on the outer slope of coral reefs in Palau, Micronesia, over a period of two years and nine months. We tagged 39 sharks (mostly adult females) of which 31 were detected regularly throughout the study. Sharks displayed strong inter-annual residency with greater attendance at monitored sites during summer than winter months. More individuals were detected during the day than at night. Mean depths of tagged sharks increased from 35 m in winter to 60 m in spring following an increase in water temperature at 60 m, with maximum mean depths attained when water temperatures at 60 m stabilised around 29°C. Sharks descended to greater depths and used a wider range of depths around the time of the full moon. There were also crepuscular cycles in mean depth, with sharks moving into shallower waters at dawn and dusk each day. We suggest that daily, lunar and seasonal cycles in vertical movement and residency are strategies for optimising both energetic budgets and foraging behaviour. Cyclical patterns of movement in response to environmental variables might affect the susceptibility of reef sharks to fishing, a consideration that should be taken into account in the implementation of conservation strategies.

Dynamic stability of coral reefs on the west Australian coast.

Monitoring changes in coral cover and composition through space and time can provide insights to reef health and assist the focus of management and conservation efforts. We used a meta-analytical approach to assess coral cover data across latitudes 10-35°S along the west Australian coast, including 25 years of data from the Ningaloo region. Current estimates of coral cover ranged between 3 and 44% in coral habitats. Coral communities in the northern regions were dominated by corals from the families Acroporidae and Poritidae, which became less common at higher latitudes. At Ningaloo Reef coral cover has remained relatively stable through time (∼28%), although north-eastern and southern areas have experienced significant declines in overall cover. These declines are likely related to periodic disturbances such as cyclones and thermal anomalies, which were particularly noticeable around 1998/1999 and 2010/2011. Linear mixed effects models (LME) suggest latitude explains 10% of the deviance in coral cover through time at Ningaloo. Acroporidae has decreased in abundance relative to other common families at Ningaloo in the south, which might be related to persistence of more thermally and mechanically tolerant families. We identify regions where quantitative time-series data on coral cover and composition are lacking, particularly in north-western Australia. Standardising routine monitoring methods used by management and research agencies at these, and other locations, would allow a more robust assessment of coral condition and a better basis for conservation of coral reefs.